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. 2024:31:63.
doi: 10.1051/parasite/2024064. Epub 2024 Oct 8.

Novel gene arrangement in the mitochondrial genome of Aspersentis megarhynchus (Acanthocephala, Echinorhynchida, Heteracanthocephalidae), and its phylogenetic implications

Yuan-Yuan Xie  1 , Hui-Xia Chen  2 , Tetiana A Kuzmina  3 , Olga Lisitsyna  3 , Liang Li  1
Affiliations

Novel gene arrangement in the mitochondrial genome of Aspersentis megarhynchus (Acanthocephala, Echinorhynchida, Heteracanthocephalidae), and its phylogenetic implications

Yuan-Yuan Xie et al. Parasite. 2024.

Abstract
in English, French

The Heteracanthocephalidae Petrochenko, 1956 is a rare family of acanthocephalans mainly parasitic in fishes. The pattern of mitogenomic evolution of the Heteracanthocephalidae is still unknown, and the phylogenetic relationships of the Heteracanthocephalidae with the other 14 families within the order Echinorhynchida remain unclear. In the present study, the complete mitochondrial genome of Aspersentis megarhynchus (von Linstow, 1892) Golvan, 1960 was sequenced and annotated for the first time, which represents the first mitogenomic data for the genus Aspersentis and also for the family Heteracanthocephalidae. The mitogenome of A. megarhynchus has 14,661 bp and includes 36 genes, containing 12 protein-coding genes (PCGs) (missing atp8), 22 tRNA genes, and 2 ribosomal RNAs (rrnS and rrnL), plus two non-coding regions. Comparative mitochondrial genomic analysis revealed that the presence of translocations of several tRNA genes (trnV, trnE, and trnT) and the gene arrangement in the mitogenome of A. megarhynchus represents a new type in Acanthocephala. Moreover, the mitogenomic phylogenetic results based on concatenated amino acid sequences of 12 protein-coding genes strongly supported the validity of the Heteracanthocephalidae and suggested close affinity between the Heteracanthocephalidae and Echinorhynchidae in the order Echinorhynchida.

Title: Nouvel arrangement de gènes dans le génome mitochondrial d’Aspersentis megarhynchus (Acanthocephala, Echinorhynchida, Heteracanthocephalidae) et ses implications phylogénétiques.

Abstract: Les Heteracanthocephalidae Petrochenko, 1956 sont une famille rare d’acanthocéphales principalement parasites de poissons. Le schéma d’évolution mitogénomique des Heteracanthocephalidae est encore inconnu, et les relations phylogénétiques des Heteracanthocephalidae avec les 14 autres familles de l’ordre Echinorhynchida restent floues. Dans la présente étude, le génome mitochondrial complet d’Aspersentis megarhynchus (von Linstow, 1892) Golvan, 1960 a été séquencé et annoté pour la première fois, ce qui représente les premières données mitogénomiques pour le genre Aspersentis et également pour la famille Heteracanthocephalidae. Le mitogénome d’A. megarhynchus compte 14 661 pb et comprend 36 gènes, contenant 12 gènes codant pour des protéines (atp8 manquant), 22 gènes d’ARNt et 2 ARN ribosomiques (rrnS et rrnL), plus deux régions non codantes. L’analyse génomique mitochondriale comparative a révélé que la présence de translocations de plusieurs gènes d’ARNt (trnV, trnE et trnT) et la disposition des gènes dans le mitogénome d’A. megarhynchus représentent un nouveau type chez les Acanthocephala. De plus, les résultats phylogénétiques mitogénomiques basés sur des séquences concaténées d’acides aminés de 12 gènes codant pour des protéines soutiennent fortement la validité des Heteracanthocephalidae et suggèrent une affinité étroite entre les Heteracanthocephalidae et les Echinorhynchidae dans l’ordre des Echinorhynchida.

Keywords: Acanthocephala; Heteracanthocephalidae; Mitochondrial genome; Nototheniidae; Phylogeny.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1
Photomicrographs of Aspersentis megarhynchus collected from Notothenia coriiceps. A: mature male; B: proboscis; C: eggs; D: mature female.
Figure 2
Figure 2
Gene map of the mitochondrial genome of Aspersentis megarhynchus. All 22 tRNA genes are nominated by the one-letter code with numbers differentiating each of the two tRNAs, serine and leucine. All genes are transcribed in the clockwise direction on the same strand. The outermost circle shows the GC content and the innermost circle shows the GC skew.
Figure 3
Figure 3
Relative synonymous codon usage (RSCU) of Aspersentis megarhynchus. The codon families (in alphabetical order) are labelled on the x-axis. Values on the top of each bar represent amino acid usage in percentage.
Figure 4
Figure 4
Comparison of the linearized mitochondrial genome arrangement for acanthocephalans species. All genes are transcribed in the same direction from left to right. The tRNAs are labelled by a single-letter code for the corresponding amino acid. Aspersentis megarhynchus is indicated using an asterisk (*).
Figure 5
Figure 5
Phylogenetic analyses of Acanthocephala inferred from the ML and BI methods based on concatenating amino acid sequences of 12 protein-coding genes (PCGs) of mitochondrial genome. Rotaria rotatoria and Philodina citrina are the out-group. Aspersentis megarhynchus is indicated using an asterisk (*).
<i>Supplementary file 2</i>:
Supplementary file 2:
The predicted secondary structures of 22 tRNAs in the mitogenome of Aspersentis megarhynchus (Watson-Crick bonds indicated by lines, GU bonds indicated by dots, red bases representing anticodons). The tRNAs are labelled with the abbreviations of their corresponding amino acids according to the IUPAC-IUB code.
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